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Bacteriophage Applications for Food Production and Processing

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Bacteriophage Applications for Food Production and Processing viruses Review Bacteriophage Applications for Food Production and Processing Zachary D. Moye *, Joelle Woolston and Alexander Sulakvelidze Intralytix, Inc., The Columbus Center, 701 E. Pratt Street, Baltimore, MD 21202, USA; [email protected] (J.W.); [email protected] (A.S.) * Correspondence: [email protected] Received: 19 March 2018; Accepted: 11 April 2018; Published: 19 April 2018 Abstract: Foodborne illnesses remain a major cause of hospitalization and death worldwide despite many advances in food sanitation techniques and pathogen surveillance. Traditional antimicrobial methods, such as pasteurization, high pressure processing, irradiation, and chemical disinfectants are capable of reducing microbial populations in foods to varying degrees, but they also have considerable drawbacks, such as a large initial investment, potential damage to processing equipment due to their corrosive nature, and a deleterious impact on organoleptic qualities (and possibly the nutritional value) of foods. Perhaps most importantly, these decontamination strategies kill indiscriminately, including many—often beneficial—bacteria that are naturally present in foods. One promising technique that addresses several of these shortcomings is bacteriophage biocontrol, a green and natural method that uses lytic bacteriophages isolated from the environment to specifically target pathogenic bacteria and eliminate them from (or significantly reduce their levels in) foods. Since the initial conception of using bacteriophages on foods, a substantial number of research reports have described the use of bacteriophage biocontrol to target a variety of bacterial pathogens in various foods, ranging from ready-to-eat deli meats to fresh fruits and vegetables, and the number of commercially available products containing bacteriophages approved for use in food safety applications has also been steadily increasing. Though some challenges remain, bacteriophage biocontrol is increasingly recognized as an attractive modality in our arsenal of tools for safely and naturally eliminating pathogenic bacteria from foods. Keywords: bacteriophages; phages; food safety; foodborne illness 1. Introduction From leaves of lettuce and cheddar cheese in a Cobb salad to frozen pre-cooked meals, the foods we eat remain under constant threat of contamination by microbial pathogens, which can subsequently be transmitted to the consumer. Recently, the Foodborne Disease Burden Epidemiology Reference Group (FERG) was established by the World Health Organization (WHO) to monitor foodborne illness across the world. FERG monitored the 31 foodborne pathogens that caused the highest morbidity and mortality in humans. In their most recent (2015) estimate of the global burden of foodborne illness, FERG approximated that 600 million foodborne infections occurred in 2010, resulting in over 400,000 deaths. Of the top five microorganisms causing foodborne illness, four were bacteria: Escherichia coli (~111 million), Campylobacter spp. (~96 million), non-typhoid Salmonella enterica (~78 million), and Shigella spp. (~51 million), with estimates for the number of foodborne-related deaths caused by these bacteria ranging from ~15,000 for Shigella spp. to ~63,000 for E. coli [1]. Strikingly, children under five years old were disproportionally impacted; they account for 40% of deaths while representing just 9% of the world population [1]. These foodborne illnesses are also a tremendous drain on the economy of nations; for example, in the United States the average incident is estimated to Viruses 2018, 10, 205; doi:10.3390/v10040205 www.mdpi.com/journal/viruses Viruses 2018, 10, 205 2 of 22 cost ~$1500/person, with the total annual estimated cost of these foodborne diseases reaching over $75 billion [2]. Several approaches are used to help improve the safety of our foods. Heat pasteurization is commonly used to reduce bacterial numbers in liquids and dairy items, most notably milk. However, pasteurization is not suitable for many fresh food items, as the process results in the items being cooked. Another method used to reduce pathogens in foods is High Pressure Processing (HPP) which exposes foods to high pressure to inactivate microbes. This technique has been successfully used on liquid products and pre-cooked meals, meant to be frozen; however, as with heat pasteurization, it is generally not used with fresh meats and produce, as it can affect the appearance (color) and/or nutritional content of these products [3,4]. Irradiation is also an effective means for reducing the burden of pathogenic organisms in foods. However, irradiation can deleteriously affect the organoleptic qualities of foods; in addition, customer acceptance of this method is low and is compounded by a labelling requirement for many food items treated with radiation [5,6]. Finally, chemical sanitizers, such as chlorine and peracetic acid (PAA), are commonly utilized to reduce microbial contaminants of many fresh fruits and vegetables as well as Ready-To-Eat (RTE) food products [7,8]. While they are, in general, effective, many of these chemicals are corrosive and can damage food processing equipment. Chemical sanitizers can also deleteriously affect the environment (i.e., not environmentally-friendly) and, with the current trends toward chemical-free, organic foods, consumer acceptance of chemical additives in foods (particularly in fresh produce) is declining rapidly. One common downside shared by all of these techniques is that they kill microbes indiscriminately; in other words, both the pathogenic as well as potentially advantageous normal flora bacteria are targeted equally. Additionally, even with the variety of methods available, foodborne outbreaks still occur relatively frequently. These factors combined illustrate the need for a targeted antimicrobial approach, one that can be used alone or in combination with the techniques described above, to establish additional barriers in a multi-hurdle approach to preventing foodborne bacterial pathogens from reaching consumers. One such technique is the use of lytic bacteriophages for targeting specific foodborne bacteria in our foods, without deleteriously impacting their normal—and often beneficial—microflora. This approach is termed “bacteriophage biocontrol” or “phage biocontrol”. Phage biocontrol is increasingly accepted as a natural and green technology, effective at specifically targeting bacterial pathogens in various foods, in order to safeguard the food chain (Table1). Bacteriophages were first identified by Felix d’Herelle in 1917, and the usefulness of these “bacteria eaters” for combating bacterial diseases was quickly exploited [9]. In the context of food safety, bacteriophages address many of the concerns voiced by consumers. For example, because of the specificity of bacteriophages, phage biocontrol offers a unique opportunity to target pathogenic bacteria in foods without disturbing the normal microflora of foods. Of note, the United States Army recently initiated a project (W911QY-18-C-0010) to further elucidate the impact of phage application versus traditional chemical antimicrobials on the normal microbiota of fresh produce and how these interventions may impact the nutritional value of foods. Also, phage biocontrol is arguably the most environmentally-friendly antimicrobial intervention available today. Most, if not all, currently-available commercial phage biocontrol products contain natural phages, i.e., phages isolated from the environment, that are not genetically modified. Many of these preparations also do not contain any additives or preservatives; they are typically water-based solutions consisting of purified phages and low levels of salts. Several phage preparations on the market are also certified Kosher and Halal and are available for use in organic foods (OMRI-listed in USA; SKAL in EU) (Table2). Although there is limited testing, work conducted by our group suggests that bacteriophages do not alter the organoleptic (i.e., sensory) properties of foods [10]. Finally, compared to other food safety interventions, the cost of applying bacteriophages is relatively low and is typically in the range of 1–4 cents per pound of food treated; whereas HPP treatment and irradiation typically cost 10–30 cents per pound [11]. It is important to note that these figures represent the cost of each intervention alone, and do not account for situations where a multi-hurdle approach may be required for food safety purposes (e.g., foods are Viruses 2018, 10, 205 3 of 22 feared to be contaminated by more than one foodborne pathogen) or for considerations apart from food safety (e.g., food spoilage which is typically caused by multiple different microorganisms). The biological properties of lytic bacteriophages and other qualities of commercial phage biocontrol products as explained above make phage biocontrol a very attractive modality for further improving the safety of our foods, and an increasing number of companies worldwide are engaging in their development and commercialization [12] (Table2). However, phage biocontrol does have its limitations and drawbacks. For example, phage preparations require refrigerated storage (typically 2–8 ◦C), and if used in conjunction with chemical sanitizers, may need to be applied separately, as harsh chemicals can also inactivate the phage particles and render phage biocontrol less effective. Also, because of their high natural specificity, phage preparations can effectively address targeted pathogens in foods, but if food
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